PBR1 selectively controls biogenesis of photosynthetic complexes by modulating translation of the large chloroplast gene Ycf1 in Arabidopsis

Abstract

The biogenesis of photosystem I (PSI), cytochrome b6f (Cytb6f) and NADH dehydrogenase (NDH) complexes relies on the spatially and temporally coordinated expression and translation of both nuclear and chloroplast genes. Here we report the identification of photosystem biogenesis regulator 1 (PBR1), a nuclear-encoded chloroplast RNA-binding protein that regulates the concerted biogenesis of NDH, PSI and Cytb6f complexes. We identified Ycf1, one of the two largest chloroplast genome-encoded open reading frames as the direct downstream target protein of PBR1. Biochemical and molecular analyses reveal that PBR1 regulates Ycf1 translation by directly binding to its mRNA. Surprisingly, we further demonstrate that relocation of the chloroplast gene Ycf1 fused with a plastid-transit sequence to the nucleus bypasses the requirement of PBR1 for Ycf1 translation, which sufficiently complements the defects in biogenesis of NDH, PSI and Cytb6f complexes in PBR1-deficient plants. Remarkably, the nuclear-encoded PBR1 tightly controls the expression of the chloroplast gene Ycf1 at the translational level, which is sufficient to sustain the coordinated biogenesis of NDH, PSI and Cytb6f complexes as a whole. Our findings provide deep insights into better understanding of how a predominant nuclear-encoded factor can act as a migratory mediator and undergoes selective translational regulation of the target plastid gene in controlling biogenesis of photosynthetic complexes.

Protein import into chloroplasts and its regulation by the ubiquitin-proteasome system

“…However, analysis of tic56 mutants attributed the observed phenotypes to defects in ribosome assembly, and revealed no impairment of protein import [88][89][90][91], a result shared when ycf1 translation was repressed by the specific plastid ribosomal inhibitor spectinomycin [92]. Tic214 has also been found to have functions in the biogenesis of photosynthetic complexes in thylakoid membranes [93], which may contribute to the severity of its knock-out phenotype. It is plausible that the 1 MDa TIC components act in multiple processes, including protein import, with additional machinery operating either in series or in parallel.…”

Overexpression of the RieskeFeS Protein Increases Electron Transport Rates and Biomass Yield

“…Although there are many examples of coordination of the accumulation of photosynthetic complexes in the thylakoid membrane, the underlying regulation of the synthesis and assembly of components of the thylakoid membrane, the factors determining the accumulation of these complexes, is still poorly understood (Schöttler et al, 2015). Recently, a nucleus-encoded chloroplast RNA-binding protein, photosystem biogenesis regulator1 (PBR1), was identified and shown to be involved in the coordination of the biogenesis of the PSI, cyt b 6 f, and NDH complexes (Yang et al, 2016). It will be interesting to explore the role of PBR1 in the plants produced in this study, as these are likely useful tools to investigate fundamental questions on factors controlling both the biogenesis and activities of the photosynthetic complexes in the electron transport chain.…”

Exploring evolution characteristic between cultivated tea and its wild relatives using complete chloroplast genomes

“…Because of photosystem biogenesis regulator 1 (PBR1), the RNA binding protein encoded by the nuclear genome, can improve the translation e ciency of ycf1 in Arabidopsis thaliana cp genome. Then, the symbiosis and stability maintenance of the three photosynthetic complexes were regulated [45]. However, at present, the effect of the mutation in the single amino acid site and insertion or deletion of the short sequence on the function of ycf1 is still not clear, and cultivated tea may be ideal materials for this kind of research.…”